Environmental biology of fishes, tập 91, số 4, 2011

References Armstrong DA, Rooper C, Gunderson DR 2003 Estuarine production of juvenile Dungeness crab Cancer mgister and contribution to the Oregon-Washington coastal Banas NS, Hickey BM

Age and growth of the small red scorpionfish, Scorpaena

notata Rafinesque, 1810, based on whole and sectioned

otolith readings

Giuseppe Scarcella&Mario La Mesa&

Fabio Grati&Piero Polidori

Received: 12 March 2010 / Accepted: 16 March 2011 / Published online: 1 April 2011

# Springer Science+Business Media B.V 2011

Abstract Age and growth of Scorpaena notata from

the northern Adriatic Sea were investigated by annual

growth increment counts (annuli) Overall, age and

growth were estimated from 538 specimens of S

notata ranging between 47 and 199 mm TL No clear

sexual dimorphism in size was observed Annual

deposition of annuli and location of the first annulus

have been validated by edge analysis and daily

growth increment counts, respectively The estimated

age range was between 0–16 years for female and 0–

14 years for males The estimated values of Von

Bertalanffy asymptotic length L1 (cm) and k

(years−1) were 16.3 and 0.46 for males and 15.6 and

0.35 for females Thus, males of S notata appeared to

attain a slightly larger size at faster rate than females

The growth performance index ranged between 1.9

and 2.1, which is in the middle of the range observed

in other scorpaenids Comparing ageing data of S

notata with other Mediterranean scorpaenids, a direct

relationship between fish size and growth performance

was observed

Keywords Adriatic Sea Age and growth

Scorpaenidae Scorpaena notata

Introduction

The small red scorpionfish, Scorpaena notata (Rafinesque1810) (Pisces, Scorpaenidae), is a benthic sedentaryspecies distributed in the Eastern Atlantic from theBay of Biscay to Senegal, off Madeira, Azores andthe Canary Islands, in the Mediterranean Sea and theBlack Sea, where it is represented by the subspeciesScorpaena notata afimbria (Slasteneko 1939) (Hureauand Litvinenko 1986) Although S notata is consid-ered to be rare in the northern Adriatic Sea (Hureauand Litvinenko1986), it was frequently found in recentsurveys close to natural and artificial hard bottom (Fabi

et al 2004; Casellato and Stefanon 2008), playinglikely a more important role in the benthic fishcommunity of rocky habitat than previously thought.The small red scorpionfish is generally less than

20 cm total length (TL), and inhabits preferably rockybottoms inside crevices or sea grass meadows, but it

is also captured by trawlers operating on sandybottoms in the proximity of hard substrates (Hureauand Litvinenko 1986; Harmelin-Vivien et al 1989;Morte et al.2001; Relini et al.2007)

Several biological aspects of S notata have beenstudied in the Mediterranean Sea, such as diet(Harmelin-Vivien et al 1989; Morte et al 2001),gonad morphology (Muñoz et al 1996, 2002a, b),fecundity and reproductive cycle (Muñoz et al.2005)and the relationships with artificial and naturalhabitats (Relini et al 2002; Ordines et al 2009).The only data concerning age and growth are

DOI 10.1007/s10641-011-9796-0

Istituto di Scienze Marine,

Consiglio Nazionale delle Ricerche,

L.go Fiera della Pesca 2,

60125 Ancona, Italy

e-mail: g.scarcella@ismar.cnr.it

presented in a publication based on scales reading of

specimens from the Gulf of Gabes (Bradai and

Bouain1990) and by a recent study of Ordines et al

(2009) about the habitat preference of S notata in

Balearic Islands

The present paper aims to improve the knowledge

of ageing procedure for S notata by means of otolith

readings, also observed after sectioning, in order to

reach a better understanding of the life span and the

calculation of the Von Bertalanffy growth parameters

of the species, applying also indirect age validation

methods to support the reliability of age estimates

Material and methods

Samples of S notata were collected in the northern

Adriatic Sea between July 2004 and November 2008

The study area included both natural reefs consisting

of hard substrates and artificial structures, such as

off-shore gas platforms (Fig.1) Sampling was carried out

in the proximity of natural reefs and artificial

structures, using a beam trawl with 40 mm cod-end

stretched mesh size and trammel nets with 70 and

400 mm stretched mesh size Hauls performed with

beam trawl were randomly located over the whole

sampling area The beam trawl was generally towed at

about 4.8–5.2 knots for 15–30 min on the bottomduring daylight hours Conversely, trammel nets,positioned close to artificial structures and naturalreefs, were set at dusk and pulled in at dawn, with anaverage fishing time of 12 h

The size distribution of the sample could beaffected by the selectivity of the gears employed.Anyway, the beam trawl was towed at a speed of sixknots and, hence, its selectivity was strongly reduced

by the scarce opening of codend meshes It isacknowledged that codends of such gears are virtuallynon-selective for the sizes of most finfish (Rotherham

et al 2008) In addition, the particular shape of S.notata (round body with many spines) stronglyreduces the probabilities of escaping thoughout thecodend meshes

A study on gillnet selectivity carried out inMediterranean showed that this gear is scarcelyselective for Scorpaena porcus (Stergiou and Erzini

2002) As a matter of fact, trammel nets are widelyconsidered less selective if compared to gillnets, and,also in this case, the presence of many spines aroundthe body of scorpenids favour the non-selective way

of capture called“entanglement” On this basis, it can

be realistic to assume that the samples collectedduring fishing survey may be representative of thepupulation at sea

Fig 1 Map of northern Adriatic Sea with sampling locations

In the laboratory, wet weight (W, 0.1 g), TL,

measured to the lowest mm, and sex, determined by

macroscopic examination of gonads were recorded for

each specimen In small specimens, gonads were

observed by a light microscope to aid sex determination

The sagittal otoliths were removed from all specimens,

cleaned and stored dry

The length–weight relationship of fish was

calcu-lated both for the whole population and for each sex

The exponential equation W=aTLb, where W is total

weight (0.1 g), TL is total length of fish (mm) and a

and b are regression parameters, was fitted to the data

The equation was linearized applying the log10

transformation of data to estimate the regression

parameters An F-test was used to test for difference

between males and females in allometric indices (b)

(Sokal and Rohlf1995)

The weight of both left and right sagitta was

recorded with an accuracy of 0.1 mg and compared

using a t-test for paired comparisons (Sokal and Rohlf

1995) As no difference was found (Student’s t-test, d

f.=806, t=1.647, p>0.05), the maximum (ODmax;

0.01 mm) and the minimum diameter (ODmin;

0.01 mm) were measured from one randomly selected

sagitta (left or right) on the whole sample, under a

stereomicroscope coupled to a video camera using an

image analysis software (OPTIMAS 6.5) The

rela-tionship between TL and ODmax and ODmin was

investigated by linear regression analysis

Otoliths were immersed in ethanol with distal face

up and the annuli were counted using a binocular

microscope under reflected light against a dark

background (magnification: ×25 and ×40) The

nucleus and the opaque zones of otolith appeared as

light rings and the translucent or hyaline zones as

dark rings The combination of each opaque and

subsequent translucent zone was considered to be an

annulus, as observed in other scorpaenids (Massutí et

al.2000; López Abellán et al.2001)

In larger fish, the annulation pattern was difficult to

discriminate due to considerable otolith thickness As

a consequence, these otoliths were embedded in

epoxy resin and transversally sectioned Otolith

sections were then polished with 0.05 μm alumina

paste and read under reflected light following the

same aforementioned procedure To compare the two

readings procedures also in smaller otoliths, a

representative sample of them was read directly as a

whole and then sectioned As the age estimates were

the same, the sectioning practice was carried out only

on the thick otoliths of larger (older) fish

The count path of annuli in whole otoliths wasgenerally from the nucleus towards the tip of therostrum, where the deposition of seasonal ringsappeared to start Otoliths were firstly read by onereader, without any ancillary data on fish size Asecond reading was carried out a week later by thesame reader

When readings differed by one or more annuli, athird reading was made; if the third reading differedfrom the previuos two, the otolith was discarded Theindex of average percent error (APE) (Beamish andFournier 1981), as well as the mean coefficient ofvariation (CV) (Chang 1982), were calculated toestimate the relative precision between readings

To assess the annual nature of ring deposition, i.e theaccuracy of age estimates, two different indirect or semi-direct methods were applied To validate specimensaged 0, i.e fish with sagittae composed of only anopaque nucleus, some otoliths were randomly selectedfor microincrements (daily rings) counting Followingother studies on scorpaenids (Laidig and Ralston1995;Massutí et al.2000), we assumed that microincrementswere laid down daily, providing the true age (in days)

of aged specimens Otoliths were set in moulds,embedded in epoxy resin and ground to obtain sagittalsections They were then polished with 0.05 μmalumina paste and the microincrements counted under

a light microscope at magnification ×400–630

To validate the seasonality of deposition of opaqueand translucent zones, the relative frequency of anopaque zone on the otolith margin was plotted bymonth (Beckman and Wilson 1995; Panfili andMorales-Nin 2002) The cycle in formation of theopaque and translucent zones should equal 1 year intrue annuli (Campana2001)

Once the age estimates were validated, the VonBertalanffy growth function was fitted to the age-length data using the routine FISHPARM from thestatistical package FSAS (Saila et al 1988), whichimplements the Marquardt algorithm for non-linearleast squares parameter estimation The Von Bertalanffygrowth parameters (L1, k and t0) were calculated foreach sex and for the whole population (includingunsexed fish) Finally, the growth performance index(Ф′=2 log L1þ logk) (Munro and Pauly 1983), wascalculated to compare the growth of S notata withother scorpaenids

Overall, 570 specimens of S notata were collected, 239

females, 302 males and 29 unsexed individuals The

sex ratio differed significantly from 1:1, males being

more abundant than females (χ2

=7.3, d.f.=1, p<0.01)

Males and females had similar size ranges, 65 to

198 mm and 47 to 199 mm, respectively, and size

range of unsexed fish was between 75 and 155 mm

(Fig 2) Individual fish weights varied between 1.7

and 169.0 g for females and between 5.4 and 143.7 g

for males

The relationships between TL (mm) and W (0.1 g)

was calculated for each sex and for the whole

population including unsexed fish, as summarized in

the following equations:

W¼ 0:000017TL3:07; n ¼ 239; r2¼ 0:97 females

W¼ 0:000016TL3:09; n ¼ 302; r2¼ 0:98 males

W¼ 0:000017 TL3:08; n ¼ 570; r2¼ 0:96 total

The coefficient b was not significantly different

between sexes (F-test, F1–536=0.236, p>0.1), and

nearly isometric

Maximum and minimum otolith diameters (ODmax,

ODmin) varied linearly with fish length, according to

the following equations:

ODmax ¼ 0:47 TL þ 0:55; n¼ 570; r2¼ 0:89

ODmin¼ 0:17 TL þ 0:65; n¼ 570; r2¼ 0:76

The annulation pattern of otoliths was composed of

alternating opaque and translucent zones Outside the

opaque nucleus, the first 2–3 rings were wide and

easily recognizable, followed by rings of decreasing

thickness towards the otolith margin (Fig.3) In larger

fish (>150 mm), the outer rings close to the margin

were difficult to discriminate, so the transversesections were helpful to obtain a more reliable count

of annuli (Fig.4)

Microincrement counts to validate fish aged 0 (i.e.young of the year) were carried out on ten specimensranging between 47 and 96 mm TL The sagittae of S.notata showed the typical pattern of light and darkalternated microincrements, representing daily growthrings (Fig.5) A continuous series of concentric rings

of increasing size, ranging from 1.0 to 3.6 μm, wereobserved from the core to the otolith margin.Accessory primordia were also observed in somespecimens The age estimates ranged from 140 to

300 days, validating all otoliths aged 0 characterized

by an opaque nucleus surrounded by a more or lessdeveloped translucent zone

Fig 3 Photograph showing the annulations pattern of Scorpaena notata sagittal otolith, 3-years-old male, 112 mm total length (TL)

Fig 2 Length frequency distribution of Scorpaena notata

sampled in the northern Adriatic Sea

Fig 4 Photographs of (a) surface and (b) cross-section otolith

of Scorpaena notata, 16-years-old female, 165 mm total length (TL) Vertical line indicate plane observed by cross-section Dots denote annulus from 1st to 16th

The edge analysis, performed on the whole fish

sample, validated the annual deposition of each

annulus formed by an opaque and translucent zone

In particular, the opaque zones were laid down from

April to August, whereas the translucent zones were

laid down from September to March (Fig.6)

Out of 570 otoliths examined, only 32 (approximately

5%) were discarded, because they were either

unreadable or provided different age estimates

between readings Counting variability indices, CV

and APE, were both quite low (11.6% and 8.2%,

respectively), indicating that the ageing procedure

adopted gave a reasonable level of consistency (or

reproducibility) between readings

Age estimates ranged between 0 and 14 years for

males and between 0 and 16 years for females

(Table 1) However, the fish sample was mainly

composed of 1–4-year-old fish, representing 80% and

72% of males and females, respectively The VonBertalanffy growth function was fitted to the age-length data pairs for each sex, and for the wholepopulation (Table2, Fig.7) The parameters estimatedwere significantly different between sexes only ifconsidered together, with male showing L1, k and t0slightly higher than females (Table 3) The growthperformance index (Ф′), calculated for each sex, isreported in Table 2 Lengths-at-age, calculated fromthe Von Bertalanffy growth function, provides esti-mates of growth increments by age The annualgrowth rate ranged between 19.2 and 0.2 mm forfemales and 28.8 and 0.1 mm for males in theestimated age range (Table 4)

Discussion

Comparing the results of the age reading reported inthe present paper with those obtained in otherpublished works on small red scorpionfish, it ispossible to discover evident discrepancies (Table 2).The ageing methodology (scales reading) adopted byBradai and Bouain (1990), as well as the relativelynarrow fish size range composed of small individuals,could have led to an underestimate of the life span of

S notata from the Gulf of Gabes Indeed, differentlyfrom scales, otoliths are one of the few calcifiedstructures that is nonskeletal and their growth ismaintained even through periods when somaticgrowth is nonexistent (Maillet and Checkley 1990;Campana and Thorrold 2001) The advantage of acontinuous growth pattern is most evident in studies

of old fish, in which annulus counts from scalesgrossly underestimate those visible in the otolith(Beamish and McFarlane 1995) Instead, the studyfrom Balearic Islands (Ordines et al.2009) was based

on otolith readings carried out on a large fish sample(947 individuals), characterized by a wide size rangecomparable to the Adriatic sample However, ageestimates were performed on whole otoliths, whichagain could have led to an underestimate of age inolder (larger) specimens of S notata, considering thatgenerally otoliths of these individuals are extremelyopaque and too thick to allow a reliable estimate ofrings close to the otolith margin

Interestingly, S notata did not show a clear sexualsize dimorphism in growth, although males may have

a slightly greater size at age than females This is in

Fig 6 Monthly change in relative frequency of the opaque zone

and translucent zone on the otolith margin of Scorpaena notata

Fig 5 Photomicrograph of otolith microstructure in the core

region, showing the typical pattern of alternating light and dark

Table 2 The von Bertalanffy growth parameters, number of specimens, growth performance indices ( Ф′), size and age ranges observed for Scorpaena notata The asymptotic standard errors of the estimates are shown between brackets

Authors Area Method Sex L∞mm k year−1 t 0 year n Ф′ Age ranges years Size ranges mm Present study Northern Adriatic

Table 1 Age length key of

Sorpaena notata sampled in

the northern Adriatic Sea,

and the number of fish (n)

contrast to most other Scorpaeniformes, females being

often larger than males (Wyllie Echeverria 1986;

Lenarz and Wyllie Echeverria 1991).Generally, it is

rather common in fish that a larger size in females

increase their fecundity, while the same may not be

true in males (Berglund et al.1986) In the case of S

notata, the documented low fecundity (Muñoz et al

2005), compared to other Scorpaeniformes, such as

Trigla lyra (Muñoz2001) or H dactylopterus (Muñoz

and Casadevall 2002), could be the reason of theabsence of sexual size dimorphism

As reported for H dactylopterus (Massutí et al

2000), S notata exhibited a double mechanism offormation of seasonal growth rings, corresponding todifferent stages of life, namely immature/juvenile andadult fish The change in deposition pattern was

Fig 7 von Bertalanffy growth curves fitted to the length-age data

of Scorpaena notata a males, b females and c whole sample

Table 3 Likelihood ratio test comparison of Von Bertalanffy parameters estimated for males and females of Scorpaena notata sampled in the northern Adriatic Sea d.f = degree of

observed at about 2–3 years, in concomitance with the

attainment of first sexual maturity, which in the

northern Adriatic Sea population took place between

10 and 14 cm TL (G Scarcella, pers comm.)

Furthermore, we frequently found false rings within

the first 3–4 true annuli, as commonly observed in

some species of Helicolenus (Massutí et al 2000;

Sequeira et al 2009) Similarly, the need of otolith

sectioning for ageing purposes has been already

reported for other scorpaenids, such as Scorpaena

elongata (Gancitano and Ragonese 2008),

Helicole-nus dactylopterus (White et al 1998; Allain and

Lorance 2000), Sebastes marinus and Sebastes

men-tella (Stransky et al.2005) The relationships between

otolith diameters and fish size was linear, as reported

for other species of Scorpaena (i.e S elongata and S

maderensis) (La Mesa et al.2005; Rizzo et al.2003)

and for some Sebastidae (Wyllie Echeverria 1987),

indicating a proportionality between the two mentioned

dimensions

The seasonal deposition of opaque and translucent

zones in the whole sample, as well as the

microincre-ment counts of young-of-the-year specimens, supported

the validation of ageing fish by counting annuli The

fall-winter deposition of the translucent zone, supposed

to occur during a slow growth period, took place when

local sea temperatures reach minimum values (Artegiani

et al 1997) The precision of age estimates was

comparable to that reported for species of similar

longevity, such as Pontinus kuhlii (López Abellán et al

2001), and within the range suggested by Campana

(2001)

Considering the Von Bertalanffy growth

parame-ters estimated for the northern Adriatic population of

S notata, the negative t0 and the low value of L1

compared to the maximum size of fish caught were

probably due to the relatively low abundance of large

and small fish in the sample Anyway, the longevity

of about 15 years can be considered a reliable

estimate of the maximum age attainable by the

species, as the maximum size of fish aged is close

to that reported in several localities of the Mediterranean

Sea (Dulcic and Kraljevic1996; Merella et al 1997;

Morey et al 2003; Karakulak et al 2006) This

estimate falls within the wide range of longevity found

in other Mediterranean scorpaenids, such as S porcus

and S maderensis, which attain respectively 11 and

5 years of age (Jardas and Pallaoro1992; La Mesa et al

2005), and S elongata and H dactylopterus, which

attain more than 30 years (Massutí et al 2001;Gancitano and Ragonese2008)

The index of growth performance (Ф′) is a usefultool for comparing the growth curves of differentpopulations of the same species and/or of differentspecies belonging to the same order (Sparre et al

1987) In Mediterranean scorpaenids, the growthperformance ranged from 1.68 in S maderensis (LaMesa et al.2005), to 2.03 in S notata (present study),2.07 in H dactylopterus (Massutí et al.2000), 2.16 in

S porcus (Jardas and Pallaoro1992), 2.41 in P kuhlii(López Abellán et al 2001) and 2.45 in S elongata(Gancitano and Ragonese 2008), indicating a directrelationship between fish size and growth performance,

as observed elsewhere in the genus Sebastes (Love et al

2002)

Management Unit and Population Dynamic Unit of ISMAR-CNR Ancona who respectively contributed to the sample collection and otoliths processing We thank also Lesley Farley for the English revision of the text and two anonymous referees for their suggestions and criticism that clearly improved an earlier version

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Occurrence and biological characteristics

in Pacific Northwest coastal estuaries

Gregory D Williams&Kelly S Andrews&

Deborah A Farrer&Gregory G Bargmann&

Phillip S Levin

Received: 14 October 2009 / Accepted: 14 March 2011 / Published online: 15 April 2011

# Springer Science+Business Media B.V (outside the USA) 2011

Abstract The broadnose sevengill shark (Notorynchus

cepedianus) is a high-order marine predator distributed

worldwide in shallow coastal waters of temperate seas

Recent reports have suggested it may be a prevalent

component of Pacific Northwest coastal estuarine

communities, although biological characteristics of

the shark population remain undocumented despite

growing interest in recreational harvest of the species

Longline sampling was conducted in Willapa Bay and

Grays Harbor, Washington, USA seasonally during

2003–2006 to collect sevengill shark size, maturity,

and sex ratio data, and establish some baseline catch rateinformation Sevengill sharks were collected on 65% oflongline sets and catches were composed of subadult andmature individuals (122–283 cm TL) of both sexes.Most male sevengill sharks were large sexually matureadults, based on external clasper calcification levels,whereas most comparably sized females were consideredsubadults, based on literature-based size-at–maturityestimates Neonates and young sharks <120 cm werenot collected, nor have they been reported in otherhistoric estuary sampling efforts Sex ratios were skewedtoward males in Willapa Bay and suggest some degree ofsexual segregation for the species, as has been shown forpopulations elsewhere We suggest sevengill sharks are alargely ignored but potentially important predator inPacific Northwest estuaries This study therefore pro-vides some of the first, basic information for guidingmanagement decisions associated with a late-maturing,slow-growing shark species in these coastal habitats

Keywords Broadnose sevengill shark Lengthfrequency Estuary Sex ratio Maturity

Introduction

Background

The harvest and bycatch of sharks has risen in recentdecades, resulting in the decline of a number ofspecies (Fowler et al.2005), particularly large species

DOI 10.1007/s10641-011-9797-z

G D Williams (*)

Pacific States Marine Fisheries Commission,

2725 Montlake Boulevard East,

Seattle, WA 98112, USA

e-mail: greg.williams@noaa.gov

Northwest Fisheries Science Center,

National Oceanic and Atmospheric Administration,

2725 Montlake Boulevard East,

Seattle, WA 98112, USA

D A Farrer

Marine Fish Program,

Washington Department of Fish and Wildlife,

PO Box 1100, La Conner, WA 98257, USA

G G Bargmann

Marine Fish Program,

Washington Department of Fish and Wildlife,

600 Capital Way N.,

Olympia, WA 98501, USA

whose low fecundity and long generation times make

them highly susceptible to overexploitation (Stevens

et al 2000) Most sharks are predators found at or

near the top of marine food webs (Cortes1999), and

some species may be important in structuring marine

communities (Myers et al 2007) Consequently,

human actions that alter shark populations have raised

concerns and prompted debate about subsequent

effects to ecosystem dynamics and stability (Stevens

et al.2000; Kitchell et al.2002; Schindler et al.2002;

Baum and Myers 2004) Ultimately, understanding

the ecology and behavior of large apex predators is

crucial to clarifying a broad range of ecosystem

interactions and is a critical component of any

rigorous ecosystem-based management plan (Pikitch

et al.2004; Levin et al.2009)

The broadnose sevengill shark Notorynchus

cepe-dianus (hereafter referred to as sevengill shark) has a

disjunct worldwide distribution and is commonly

found in shallow coastal waters, bays, and estuaries

of temperate seas (Compagno 1984) They are large

(up to 3 m) coastal predators, thought to be associated

with areas of upwelling and high biological

produc-tivity (Ebert 2003) The general ecology and

occur-rence of this species has been described in several

locations: California (Ebert1989), southern Australia

(Braccini2008), South Africa (Ebert1996), Tasmania

(Barnett et al.2010b), and Argentina (Lucifora et al

2005) In North America, sevengill sharks range from

southeast Alaska to southern Baja California, with

Humboldt and San Francisco Bays serving as

impor-tant birthing and nursery grounds (Ebert2003) Little

is known about movement patterns along the open

coast, but commercial catch records (Ebert 1989),

have suggested a seasonal pattern of migration and

residency in some California bays

Broadnose sevengill sharks have never been

consid-ered a common component of the fish community in

Pacific Northwest (PNW) coastal estuaries (Bonham

1942; Hart 1973), although recent anecdotal reports

from commercial gillnet fishermen, recreational

anglers, and unpublished Washington Department of

Fish and Wildlife (WDFW) surveys suggest they may

be much more prevalent than previously reported In

2001, WDFW biologists enacted a temporary

morato-rium on sevengill shark recreational harvest in these

estuaries (G Bargmann, WDFW, pers obs.) based on

the lack of basic information related to their

abun-dance, movement patterns, and population structure

As such, sevengill sharks represent one neglected aspect

of an otherwise relatively well-studied system, where agreat deal of research has focused on bottom-upproduction (Roegner et al 2002; Hickey and Banas

2003; Parrish et al 2003; Reusink et al 2003),especially when compared to research on upper level-predators (but see Dumbauld et al.2008)

In this study, our primary objective was to clarifybasic information on the population structure ofsevengill sharks in PNW coastal estuaries Specifically,

we summarize size frequency, maturity, and sex ratiodata, but also some additional information on catch ratesand diet At one level, the data we generate is highlyrelevant to management of sevengill shark populations,which are known elsewhere to use estuaries and bays asbirthing and nursery grounds (Ebert 1989) and areconsidered ‘highly sensitive’ to fishing mortality(Smith et al 1998) At another level, management ofthese relatively small, coastal ecosystems will also beimproved by any additional information on a top-levelpredator that has the potential for affecting a cascade oftop-down effects on the food web

Materials and methods

Study area

Willapa Bay (WB; 260 km2 MHHW) and GraysHarbor (GH; 235 km2MHHW) are intermediate sizedestuaries on the Washington coast, just north of theColumbia River estuary (Jennings et al 2003)(Fig.1) Their geography, oceanography, and ecologyare thoroughly reviewed in Emmett et al (2000),Hickey and Banas (2003), and Parrish et al (2003),respectively Both are characterized by expansiveintertidal mud and sandflats, composing over half oftheir surface area, perfused with intertidal creeks thatconnect to larger channels 10–25 m deep (Emmett et

al 2000; Hickey and Banas2003) Their phy is closely linked to upwelling in the Californiacurrent large marine ecosystem, as well as large tidalranges and highly seasonal river discharge (Banas et

oceanogra-al 2004) Though in many respects the biologicalcommunity in these estuaries has been transformed bynon-native species introduced via early aquacultureactivities (Reusink et al 2006), the systems arenonetheless recognized as diverse and seasonallyproductive (Parrish et al.2003)

Field methods

We deployed demersal longline gear from commercially

chartered fishing vessels to collect sevengill sharks over

six sampling trips from 2003 to 2006 in Willapa Bay

(WB) and Grays Harbor (GH) (Table 1; Fig 1)

Longline sets were made using a 180-m groundline

deployed along the bottom with 13.6-kg anchors and

buoys at either end Size 16/0 circle hooks were baited

with herring Clupea pallasi, chum salmon

Oncorhyn-chus keta, heads of Pacific spiny dogfish Squalus

acanthias, and, or squid Loligo opalescens Hooks

were spaced at approximately 3-m intervals along the

ground-line and were attached via 136-kg test nylon

gangion cord using stainless steel longline snaps

Sampling methods were exploratory in nature and

evolved over time to include shorter set times, different

bait types, and more productive locations, but typical

longline sets were made in the late morning at depths

that ranged from 3 m to 24 m and lasted approximately

2–3 h (Table1)

Sharks were brought to the surface and lifted intothe vessel either with an aluminum-framed meshcradle using the vessel’s boom and winch They werecarefully restrained on the deck with seawaterirrigating their gills and a wet towel shielding theireyes Sharks were then measured (precaudal length[PCL; snout to precaudal pit] and total length [TL;snout to the tip of the tail in the natural position]) andweighed For male sevengill sharks, maturity wasestimated by measuring length of the mixopterygia(claspers) from insertion to tip and visually determin-ing the degree of the inner structure’s ossification,classified as either soft and flexible or stiff andcalcified (Ebert 1989) Finally, sharks were taggedthrough the dorsal fin with uniquely numbered diskand Floy© tags before being released Time out of thewater ranged between 5 and 10 min for each shark Inaddition, any diet items regurgitated by the sharks on-board the vessel were retained, visually examined,and identified to the lowest taxonomic category Allcollection and handling methods were designed to be

Fig 1 Map of sevengill

shark, longline set locations

(stars) by year in Willapa

Bay and Grays Harbor,

Washington, USA

non-lethal and were previously reviewed and

ap-proved under WDFW and University of Washington

protocols

Biological data from longline-collected sharks

were supplemented with opportunistic collection of

live individuals from ongoing WDFW sturgeon

Acipenser spp gillnet sampling studies in 2005

(WDFW, unpublished reports) Gillnet sampling was

conducted in the summer months (June–August) over

a broader area of both bays using 275 m long, sinking

gillnets composed of three equally sized panels of

25 cm, 22 cm, and 18 cm stretch mesh Gillnets were

set for an average of approximately 60 min at depths

less than 5 m

Catch rates and biological parameters

Sevengill shark catch per unit effort (CPUE) was

expressed as the number of sharks caught,

standard-ized by the median number of hooks (35) used per set

over the duration of sampling, divided by the number

of hours the longline was in the water (sharks·h−1)

Because methods changed over time and were not

part of a balanced sampling design, our analyses were

exploratory in nature and limited to a broad

descrip-tive analysis of the effect of location (estuary) andbait type (dogfish heads or chum salmon) on CPUE

We used a linear mixed model (SYSTAT2007), withCPUE as the dependent variable, location, bait type,and location*bait type as fixed effects, and samplingtrip as a random blocking effect (covariate) Statisticalanalyses were limited to longline sets made with asingle type of bait (i.e., either dogfish or chumsalmon; no mixed bait sets; n=46; Table1)

We examined the association between length (TL)and weight (W) for all sharks weighed duringsampling; parameters a and b were estimated bygender from the power function W=a*TLb Possiblegender differences were evaluated with log-transformed length and weight data, using a general-ized linear model (GLM, SYSTAT2007) to comparethe slopes of the regression lines; logW was used asthe dependant variable, while gender, logTL, and theinteraction term gender*logTL were treated as fixedeffects (Pope and Kruse2007) Different slopes of theTL:W regression lines were indicated by a significant(P<0.05) gender*logTL interaction term

Size-frequency distributions of males and femaleswere compared using a two-sample Kolmogorov-Smirnov test (Zar 1984) For sharks captured by

Table 1 Sevengill shark longline sampling details: dates, trip

total number of longline sets, mean depth (range), mean

number of hooks per set, bait type (H=herring, D=dogfish

heads, C= chum salmon, S= squid), mean soak time, and sevengill shark catch in total number and mean (SE) CPUE

longline, we used t-tests to compare mean lengths

between estuaries (GH versus WB)

The sex ratio of sevengill sharks was examined for

the entire study period, by seasonal sampling intervals

(pooled across years by April–May, June–July, and

Aug–Sept), and by estuary (GH and WB) against the

null expectation of 1:1 using the log-likelihood ratio

test (G-test) (Zar1984)

Sevengill shark size at maturity was estimated

externally using non-invasive methods For males,

maturity was directly determined by visually

examin-ing clasper length (mm) and degree of calcification

(Holden and Raitt 1974; Ebert 1989) To determine

the length at which 50% of the male sevengill sharks

reached sexual maturity (TL50), maturity ogives were

fitted to the direct maturity data by probit analysis

based on 10 cm length (TL) intervals The probit

function was fitted by maximum likelihood and

Fieller 95% confidence limits were estimated

(SYSTAT 2007) For females, size at maturity

estimates (>220 cm TL) were based on published

literature values from sharks sampled in California

(Ebert2003) Maturity ratios of both male and female

sharks were evaluated (null expectation of 1:1 ratio,

G-test) in each estuary

Results

A total of 103 sevengill sharks were collected by

longline during six sampling periods, comprising 55

sets of gear with a total soak time of over 275 h

(Table1) Most sharks (n=88) were caught in Willapa

Bay, with the remainder (n=15) caught in Grays

Harbor Seven additional sharks were collected by

research gillnets in Willapa Bay (n=1) and Grays

Harbor (n=6) There were no verified recaptures of

externally tagged individuals Biological data were

collected only from specimens brought on board the

vessel, and therefore subsequent analyses do not

include the same sample size as the entire catch For

example, animals escaping at the surface during

long-line retrieval (i.e., “bite-offs”) were counted in the

catch, but most of their biological characteristics were

not recorded Spiny dogfish were the only other

species collected during longline sampling

Sharks were caught during every sampling trip and

CPUE ranged between 0.16 and 1.12 sharks hr−1

(Table 1) Sevengill sharks were collected on 65%

(36 of 55) of longline sets, and of these sets 61% (22 of36) had multiple sharks The lowest mean shark CPUE(0.16±0.04 SE) occurred during the first sampling trip

in 2003; although total shark catch numbers were high(n = 31), this trip was characterized by long setdurations (>16 h) (Table1) The highest mean CPUE(±SE) occurred in September 2005 in both estuaries:GH=1.12±0.78; WB=1.02±0.61 (Table 1) Sharkswere caught with every type of bait but squid.Sevengill shark CPUE was not affected by bait type(chum salmon versus dogfish heads; LMM: F1,41<0.001, P=0.98), location (F1,41=0.65, P=0.43), or thebait*location interaction (F1,41=0.011, P=0.92).The relationship between TL and W for males wasW=3.758×10−7×TL3.461 (n=29, r2=0.903) and forfemales was W=2.636×10−8×TL3.969 (n=24, r2=0.946) (Fig 2) The slope of the log transformedweight-length regression equation was greater forfemales than for males, as shown by a significantgender*TL interaction term (GLM: F1,49=10.40, P=0.002)

Sevengill sharks ranged from 122 cm to 256 cm

TL for males (n=55, mean=206.8 cm, 95% dence interval [CI] = 197.9–215.8 cm) and from

confi-138 cm to 283 cm TL for females (n=44, mean=197.5 cm, 95% CI=185.9–209.2 cm) (Fig 3) Therewas a difference in length frequency distributionsbetween males and females (Kolmogorov-Smirnovtest: D0.05,55=0.295, P<0.001), with more femalesrepresented in the 160–210 cm TL size range Sharkscollected by gillnet (n=7, mean=144.7 cm, 95% CI=133.6–155.8 cm) were predictably smaller than thosecollected by longline (n=92, mean=207.1 cm, 95%CI=200.2–214.0 cm) presumably due to the smallmesh size of gillnets targeting Acipenser spp Foranimals collected exclusively by longline, sevengillsharks from Grays Harbor (n=14, mean TL=207 cm,95% CI = 190–222 cm) were indistinguishable inlength from those in Willapa Bay (n=78, mean TL=

207 cm, 95% CI=200–215 cm; t0.05(2), 90=−0.057, P=0.95)

Of the 110 sharks collected in both estuaries, 44were female, 55 were male, and 11 were not sexed(Fig.3) The overall sex ratio of males to females was1.25:1 and not significantly different from 1:1 (log-likelihood goodness of fit test: G=1.23, degrees offreedom: v=1, P>0.25); sex ratios did not changewith seasonal sampling period (pooled across years;April–May, June–July, and Aug–Sept; G=1.33, v=2,

P>0.50) However, there were more male (n=49)

than female (n=30) sharks collected in Willapa Bay

(G=4.62, v=1, P<0.05)

All male sevengill sharks <192 cm had soft,

flexible claspers and were therefore considered

immature, whereas male sharks >202 cm were

exclusively represented by sexually mature

individu-als with calcified claspers (Fig 4) Probit analysisestimated TL50 at 196 cm (95% CI=180–209 cm)(Fig 4) Across both locations, most females (75%)were smaller individuals, considered immature based

on published studies in California (Ebert 2003),whereas most males (>65%) were considered sexuallymature, based on both the literature and direct

Total length (cm)

120 140 160 180 200 220 240 260 280 300

0 20 40 60 80 100 120 140 160

180 Fig 2 Sevengill shark total

length (cm) to weight (kg)

relationships: male (filled

circle; dotted line, n=29);

female (open circle, solid

Total length (cm)

0 1 2 3 4 5 6 7 8 9 10 11 12

Maturity (literature)

Maturity (literature)

Fig 3 Length-frequency

distribution of male (top

panel) and female (bottom

panel) sevengill sharks

caught by longline and

bars represent sharks caught

in Willapa Bay (n=79);

dark bars represent sharks

collected in Grays Harbor

(n=20) Arrows indicate

estimated minimum size at

maturity from the literature

observations (Fig 3) By location, there were more

immature than mature females at both Grays Harbor

(11 immature to 3 mature; log-likelihood goodness of

fit test: G=4.86, v=1, P<0.05) and Willapa Bay

(22:8; G=6.79, v=1, P<0.01) (Fig 5) Males at

Grays Harbor were somewhat equally represented

(4:2; insufficient sample size for significance test),

whereas we collected fewer immature than mature

males in Willapa Bay (15:34; G=7.56, v=1, P<0.01)

(Fig.5)

In four separate cases during 2005 and 2006,

sharks collected in Willapa Bay everted their

stom-achs when being handled, regurgitating their stomach

contents on the deck of the vessel In three cases,

sevengill shark (178–223 cm TL) stomachs contained

sectioned marine mammal remains (e.g., fur, flippers)

that were visually determined to be harbor seal,

Phoca vitulina richardsi No other prey items wereobserved in the diets

Discussion

This research extends information on a poorly knownshark along the PNW coast and contributes to generalknowledge of the species throughout its range Ingeneral, sevengill sharks show a variety of habitat usepatterns worldwide and do not fit neatly within either

of the nearshore shark population models recentlyreviewed by Knip et al (2010) In PNW estuaries (thisstudy) and Tasmania (Barnett et al 2010b) neonates

or young sevengill sharks <120 cm were rarely if evercollected, and birthing locations and core rearingareas remain uncertain In other locations where

Total length (cm)

100 120 140 160 180 200 220 240 260 280

0 50 100 150 200

250

0 25 50 75

100 Flexible

Calcified Percentage Mature

Clasper length not measured

Fig 4 Estimated size (cm

TL) at maturity for male

sevengill sharks: observed

inner clasper length (mm)

and calcification (flexible

claspers (immature sharks)

are indicated by filled

circles, calcified claspers

(mature sharks) by open

circles, additional sharks

with unmeasured claspers

shown at bottom of y-axis)

and maturity ogive based on

Male (immature) Male (mature) Female (immature) Female (mature)

n = 20 n = 79

Fig 5 Relative proportion

of all sevengill sharks by

sex and maturity (male data

from field observations;

female size at maturity from

literature) collected from

Grays Harbor (GH) and

Willapa Bay (WB)

sevengill sharks have been sampled with similar

methods, catches encompassed a full range of age

classes, from neonates up to large adults (Ebert1989;

Lucifora et al.2005; Braccini2008) Sevengill sharks

in California (Ebert1989) and Argentina (Lucifora et

al 2005) in particular appeared to use estuaries for

birthing and juvenile rearing functions, and generally

fit the theoretical estuarine nursery model originally

proposed by Springer (1967) In contrast, sevengill

sharks from southern Australia (Braccini 2008) and

South Africa (Ebert 1996) did not preferentially use

bays as nurseries and more closely match the

population model proposed by Knip et al (2010),

with all sizes and both sexes found throughout

nearshore coastal waters

Other biological characteristics may distinguish

sevengill sharks in PNW estuaries from populations

elsewhere and provide possible clues as to the functional

importance of these habitats Catches across both

locations were composed primarily of larger, mature

males and smaller, immature females and overall sex

ratios were skewed towards males in Willapa Bay,

suggesting some degree of sexual segregation Sexual

segregation has also been observed for sevengill

populations in Tasmania (Barnett et al 2010b) and

Argentina (Lucifora et al 2005), although in both of

these examples the positive bias was towards large

female sharks Sexual segregation is a common trait of

many elasmobranchs (Springer1967; Wearmouth and

Sims2008; Speed et al.2010) and recent studies have

suggested that mating or foraging behavior are the

most likely hypotheses to describe why it may occur in

sharks For example, Sims et al (2001) demonstrated

sexual segregation by the small-spotted catshark

Scyliorhinus canicula within a small bay (lough), and

proposed it was determined by females forming

female-only aggregations to reduce energetic demands

of mating activity This hypothesis seems to be

confirmed in laboratory studies which showed female

aggregations were particularly resilient to potential

male harassment and novel female intruders (Jacoby et

al 2010) Foraging behavior, driven by sex-related

differences in nutritional demands, has been shown to

influence sexual segregation in other species such as

seals, but remains untested in any elasmobranch

species (Wearmouth and Sims2008)

It is equally plausible the size and maturity ratio

differences we observed may simply reflect the

differ-ential growth rates of a single large cohort of sevengill

sharks using these habitats As is typical for mostviviparous shark species (Cailliet and Goldman2004),male sevengill sharks grow faster at smaller initial sizes

in the wild (Braccini et al.2010) and mature at smallersizes (150–180 cm TL) than females (220–250 cm TL;Ebert2003; Lucifora et al.2005)

Our length-weight regression analyses show theweight of females begins to diverge from that ofmales at TL >220 cm, a size corresponding to otherpublished values for the onset of female sexualmaturity (Ebert1989; Lucifora et al.2005) and whichincreases confidence in our assumption about femalesize at maturity in this population However, wefound male size at maturity (TL50=196 cm TL) wassomewhat larger than reported in other studies whereinternal reproductive structures were verified, leavingopen the question of whether the differences were real

or reflected the inaccuracy of external maturityestimates Nonetheless, basic life-history informationremains important to document for geographicallydistinct populations because the productivity potential

of some species may be adapted to local conditions,may vary among stocks of the same species, or maypoint to important demographic subcomponents of alarger metapopulation (Kritzer and Sale2006).Based on the size distribution and sex/maturity ratios

of sevengill sharks collected here, we suspect PNWestuary habitats are primarily utilized as foraging areas.Enhanced prey availability, feeding opportunities, andgrowth are a number of advantages offered to sevengillsharks by these highly productive, seasonally warmhabitats, as suggested for other species such as greensturgeon Acipenser spp (Moser and Lindley 2006),Dungeness crab Cancer magister (Armstrong et al

2003), and English sole Parophrys vetulus (Gunderson

et al.1990) Diet observations, though limited, provideadditional evidence that sevengill sharks prey here onharbor seals, which concentrate to pup in Washingtoncoastal estuaries from mid-April through June (Huber

et al.2001) In all other regions where their diets havebeen studied, sevengill sharks are high-order predatorsthat shift to an elasmobranch and marine mammal-based diet with ontogeny (Ebert 2002; Lucifora et al

2005; Braccini 2008; Barnett et al 2010a) Futureresearch focusing on movement, diet, bioenergetics,and female reproductive state are the logical next steps

in evaluating hypotheses about PNW estuarine habitatdependence, reproductive functions, and coastal popu-lation connectivity

This study represents the first documentation of

sevengill sharks in PNW coastal estuaries and

provides some context for informing management

decisions associated with this large marine predator

in nearshore coastal habitats of the northern

California current Sevengill sharks are considered

‘highly sensitive’ to fishing mortality based on their

relative ability to recover from exploitation and

may be especially vulnerable because they are

found in highly accessible coastal areas that are

susceptible to environmental disturbance (Smith et

al 1998) The sound management of fisheries and

the ecosystems that support them depends

funda-mentally on a thorough understanding of basic

biology (Dayton 2003), especially for long-lived,

upper trophic level species for which we have very

limited data and where management missteps can

have large consequences (Walker 1998; Stevens et

al.2000; Myers et al.2007) Our findings therefore

begin to fill key gaps in our basic knowledge about

regional sevengill shark populations and their role in

Pacific Northwest ecosystems, while also setting the

stage for more informed management of an

emerg-ing, recreational fishery

V Silver Spray, out of North Bend, Washington, for the safe

collection of sharks during longlining operations, and Matt

Howell, Brad James, Olaf Langness, and Steve West (WDFW)

for the data provided from shark specimens during the course of

their gillnet sampling Tom Sand at Arrowac Fisheries in

Bellingham WA graciously provided us with dogfish heads

from their processing operations to use as bait We also thank

Steve Katz and Mary Moser for their enlightening discussions,

field assistance, and fundamental role in the project Reviews

from C Harvey and several anonymous reviewers greatly

improved the quality of this manuscript.

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A review on the early life history and ecology of Japanese

sea bass and implication for recruitment

Md Shahidul Islam&Yoh Yamashita&

Masaru Tanaka

Received: 12 February 2010 / Accepted: 23 March 2011 / Published online: 13 April 2011

# Springer Science+Business Media B.V 2011

Abstract Recruitment in marine fishes is regulated

largely by the demographic changes that occur during

the early life stages; therefore, a thorough understanding

of early life stages is essential for predicting recruitment

variability in fishes Japanese sea bass (JSB), Lateolabrax

japonicus, is a coastal marine fish distributed in East

Asian coastal waters, and is regarded as highly

important for commercial and recreational fisheries, for

marine and brackish water aquaculture as well as for

stock enhancement JSB is a typical estuarine dependent

temperate fish, which spawns in shelf areas and coastal

embayments and the larvae and juveniles are dispersed

and transported into shallow nearshore habitats and

estuaries where they spend the early life In this paper,

we provide insight into the early life history and ecology

of JSB through a revision of the available informationand using the data we obtained from a relatively long-term research We review and discuss the distributionand habitat use, food and feeding, age and growth,mortality and recruitment of larval and juvenile JSB incoastal waters around Japan We extend our discussions

in all available dimensions: habitat-specific, ontogenetic,and spatio-temporal, and highlight the importance ofnursery habitats We also discuss the implications ofearly life history for recruitment of JSB as well as thepossible effects of climate change At the end, we pointout potential areas for future research

Keywords Early life history Japanese sea bass Lateolabrax japonicus Larvae and juveniles Distribution and diet Growth and mortality Nurseryhabitats Recruitment Climate change

Introduction

The abundance of exploitable fishes depends directly

on the number of recruits that join adult populationeach year Recruitment in turn is greatly influenced bythe demographic changes that occur during thepelagic larval and early juvenile stages, the period atwhich most mortality of marine fishes concentrates(Houde1997) Wide spatial and temporal fluctuations

in recruitment and year class strength are usuallyassociated with fluctuations in larval mortality and

DOI 10.1007/s10641-011-9798-y

Maizuru Fisheries Research Station,

Field Science Education and Research Center,

Kyoto University,

Maizuru, Kyoto 625–0086, Japan

e-mail: dr.md.islam@gmail.com

M Tanaka

Borneo Marine Research Institute,

University of Malaysia Sabah,

Locked Bag 2073,

88999 Kota Kinabalu, Sabah, Malaysia

Present Address:

M S Islam

Department of Aquaculture, Faculty of Fisheries,

Bangabandhu Sheikh Mujibur Rahman

Agricultural University,

Gazipur 1706, Bangladesh

population dynamics For example, year class strength

of juvenile Japanese sea bass (JSB), Lateolabrax

japonicus, has been shown to vary from ten- to

fortyfold range and is affected by the survival rate

during larval stage (Matsumiya et al 1985; Shoji

et al 2006; Shoji and Tanaka 2007a) Similar

association between early life history and variability

in recruitment has been reported in many marine,

freshwater, lacustrine, and anadromous fishes (Houde

1987; Bailey and Houde 1989; Pepin and Myers

1991; Myers et al 1997) Thus, understanding the

factors that regulate larval population dynamics is

crucial for fisheries management As the global

environmental crises intensify due to large scale

impacts such as from climate change (IPCC 2007),

we need to reconsider our knowledge on early life

history of fishes from a changing environmental

context to better understand recruitment dynamics

Temperate sea basses show circumglobal distribution

and constitute important commercial fisheries around

the world, and JSB is one of them JSB is a typical

euryhaline coastal marine fish, distributed throughout

the sea margin around Japan and south-western Korea

and is regarded as highly important species for

commercial and recreational fisheries, for marine

and brackishwater aquaculture and for marine stock

enhancement (Fushimi2001; Nip et al.2003) In other

parts of the world, temperate sea basses exhibiting

similar life history characteristics and commercial

importance include among others the Chinese temperate

sea bass Lateolabrax sp distributed along Chinese

coastal waters, striped bass (Morone saxatilis) along the

East Coast of North America and the European sea bass

(Dicentrarchus labrax) in European coastal waters

While many of the world’s wild fish stocks are

declining due to overfishing and habitat degradation,

commercial catch of JSB has been increasing since the

early 1950s Due to high growth rate in aquaculture,

temperate sea basses are popular for commercial

mariculture in winter, which have been reflected in a

dramatic increase in sea bass aquaculture in the past

years

The life history of JSB is characterized by

faculta-tive amphidromy (Tanaka and Matsumiya 1982;

Matsumiya et al.1982,1985; Ohta2004) The adults

spawn in the shelf areas during winter season

(November–February); early larvae are pelagic and

late larvae migrate to a variety of nursery habitats that

include shallow inshore areas (Hibino et al 2006,

2007), sandy or rocky shores (Kinoshita 1998),seagrass beds (Fujita et al 1988; Kanou et al 2000;Hibino et al.2002), salt marsh (Jin et al.2007), as well

as brackish estuaries (Hibino et al 1999; Islam andTanaka 2006a) Transition larvae and early juvenilesascend to low salinity and freshwater areas of rivers(Matsumiya et al 1982; Islam et al 2006a,b; Suzuki

et al 2008a, b) Juvenile JSB resides in the nurseryhabitats for varying lengths of time to become young-of-the-year and then return to the adult habitats.The early life history of migratory fishes can beparticularly challenging because the essential nurseryhabitats for juveniles are located many kilometersdistant from the spawning grounds In such species,recruitment success often depends on successfulingress into the nursery habitats Therefore, under-standing the early life history is extremely important

In this paper, we provide an account of the early lifehistory and ecology of JSB around the coastal waters

of Japan Here, we review the available literature aswell as reanalyze part of our published and unpub-lished data on larval and juvenile JSB at differentspatio-temporal scales, and discuss the implications ofthe early life history traits for recruitment of JSB Wealso discuss the possible effects of climate change onearly life history and recruitment of JSB and point outpotential areas for future research Given the impor-tance for commercial fisheries and aquaculture oftemperate sea basses, this review may be of impor-tance for further progress in the biology and manage-ment of temperate sea basses in general and of JSB inparticular

Egg and larval distribution

Information on the ecological features of spawninggrounds as well as spawning behavior and biology ofJSB are extremely limited The reported occurrenceand distribution of eggs, larvae and juveniles of JSB(Fig 1) suggests that there are several spawninggrounds of JSB in coastal waters around Japan,particularly in central and western Japan In general,spawning grounds are located in the major coastalembayments and shelf areas with water depth

of <100 m In Tango Sea, spawning occurs aroundthe Kanmuri Island which correspond to a depth ofaround 80 m (Ohmi2002) while in Ariake Bay, waterdepth at spawning ground off Shimabara Peninsula

ranges 30–40 m (Hibino et al 2007) Generally,

spawning areas are located in bay mouths where

thermohaline frontal regions are formed between the

outer water and bay water and eggs are abundantly

distributed in these regions (Watanabe 1965; Horiki

1993; Hibino et al.2007) Eggs are reported to occur

from late October to late February with the peak from

late November to late January (Watanabe1965) This

temporal range in egg occurrence is consistent with

studies that either directly investigated egg

distribu-tion (Ohmi 2002; Hibino et al 2007) or

back-calculated spawning time from daily age of larvae or

juveniles (Matsumiya et al 1985; Ohta 2004) Early

stage eggs are distributed in surface layers but are

gradually shifted to the middle of the water column as

egg development proceeds and, at the same time, eggs

are also transported shoreward from the spawning

ground (Ohmi 2002; Hibino et al 2007) Detailed

patterns in vertical distribution and spatial

transporta-tion, mortality and population dynamics as well as

hatching rates of JSB eggs in the field are unknown

While salinity of the spawning areas (>30 PSU)exhibits little variability, water temperature can be asignificant factor controlling egg survival and viabil-ity In laboratory experiment, Makino et al (2003)have reported that both egg survival and viabilitywere significantly reduced at temperatures <10°C InAriake Bay, Hibino et al (2007) found very few or noeggs in areas with temperature <10°C and shift in thespatial distribution of eggs were found to be associ-ated with reduced water temperature Overall, in fieldstudies, JSB eggs were collected from areas with arather narrow range of water temperature, from 14 to20°C Although no concrete information is available

on the effect of low or high temperature or fluctuatingtemperature on JSB egg survival and viability in thefield, laboratory experiment (Makino et al 2003)suggests that drop in temperature below 10°C maycause mass mortality of JSB eggs

Little is known on the spatio-temporal distributionpattern of larvae in relation to biotic and bioticfactors In Ariake Bay, Hibino et al (2007) collected

Fig 1 Map of Japan showing the areas where Japanese sea

bass larvae and juveniles have been reported to occur Names of

the areas and corresponding references are: a Ohara (Kinoshita

early stage larvae from mid December to mid January

and found no larvae in November and February

During a larval sampling program in January–March

2008 in Tango Sea, we collected only five larvae in

three cruises in March although plenty of larvae were

collected in January and February; however, we found

no larvae in December Larvae are mostly abundant at

the middle layer of the water column (Hibino et al

2007), suggesting that hatching takes place at the

middle layer By the time larvae hatch from the eggs,

spatial distribution expands more toward the

near-shore areas and most larvae are abundant several

kilometers shoreward from the spawning grounds

(Hibino et al 2007) Since the nursery habitats are

formed in the shallow surf zones and river estuaries

that are located 25–40 km away from the spawning

ground, the larval drift toward the nursery areas is a

directional process (Hibino et al.2007) in which the

larvae synchronize their vertical position in the water

column with the water current to gain a net shoreward

movement (Islam et al.2007) Ohmi (2002) suggested

that the gravitational circulation in estuarine regions

plays an important role in larval drift toward the

inshore nursery areas Details on the physical

mech-anisms that transport eggs and larvae toward inshore

waters are still unknown

Juvenile distribution

An important life history requirement of JSB is the

use of estuaries and shallow coastal embayments as

nursery habitats located kilometers distant from the

spawning grounds Thus, JSB larvae and juveniles

constitute a considerable proportion of the fish

assemblage in the nearshore coastal habitats in spring

Larvae and juveniles have been reported to occur in

all areas shown in Fig 1 This suggests that all sorts

of nearshore habitats (seagrass beds, rocky shores,

sandy bottoms, river estuaries) are used by JSB as

nurseries (Hibino et al 2006,2007) Late larvae and

early juveniles of JSB arrive at the nursery habitats

during late winter or early spring (February–March)

In the Ariake Bay (Kyushu Island, Japan), variations

in migratory pathways for simultaneously occurring

juveniles have been reported: some migrate upstream

to the upper estuary, while others reside in the lower

estuary (Matsumiya et al.1982,1985) or in the littoral

zone (Hibino et al 2002,2006) In early spring, late

stage larvae concentrate in large numbers at theChikugo river mouth at the upper part of the AriakeBay, and the upriver migration corresponds to thelarva-juvenile transition stage (~15 mm in standardlength; Ohta 2004) The early juveniles inhabit theupriver turbidity maximum zone (TMZ), which isformed about 15 km upstream, with turbidity as high

as ~4,000 mg l−1 (Shirota and Tanaka 1981) TheTMZ is known as areas of extraordinarily high preyconcentrations (Hibino et al.1999; Islam et al.2006a,

b, c, d; Islam and Tanaka 2006a) Studies havesuggested that upstream migration to the TMZpromotes larval growth, survival and recruitmentsuccess (Islam and Tanaka 2005, 2006a; Suzuki

et al 2008a,b) A portion of the juvenile populationascends further upstream to ingress into the freshwa-ter areas (Ohta et al 1997; Secor et al 1998) Toarrive at the upstream nursery areas, JSB juveniles use

a mechanism of selective tidal stream transport inwhich they are more abundant at the surface waterduring rising tide and at the bottom or river bankduring ebbing tide (Matsumiya et al 1982, 1985;Islam et al.2007)

A substantial portion of juvenile JSB population

is retained in the littoral zones of the nearshoreareas Distribution of these juveniles in the shallownearshore habitats is synchronized with diel tidalrhythms Hibino et al (2006) reported that JSBjuveniles make use of the flood tide to migrate to thesurf zone from offshore at sunrise; juveniles staythroughout the daytime in these shallow habitats aswas evident from the continuous high daytimeabundance, and emigrate from the surf zone at sunset.The purpose of the short distance migration towardthe surf zones appeared to be associated with feeding

on prey copepods that also showed high abundance atflood tide (Hibino et al 2006)

Importance of estuarine nursery habitats

The importance of nursery habitats for the early life ofmarine fishes, particularly for estuarine dependentspecies have been recognized worldwide (Beck et al

2001; Heck et al 2003; Dahlgren et al 2006) Assuggested by the‘nursery role hypothesis’, a habitat is

a nursery for juveniles of a particular species if itscontribution per unit area to the production ofindividuals that recruit to adult populations is greater,

on average, than production from other habitats in

which juveniles occur Although juveniles of JSB

have been reported to occur in almost all forms of

coastal and nearshore habitats (e.g., eelgrass beds,

non-eelgrass beds, tidal and intertidal sand and mud

flats, rocky shores, river estuaries etc.), the relative

importance of each of these habitats as nursery for

juvenile JSB has not been evaluated according to the

‘nursery role hypothesis’ The only exception is the

Chikugo River estuary in Ariake Bay (western Japan)

which is relatively well studied as habitat for juvenile

JSB and, based on the‘nursery role hypothesis’, is an

extremely important nursery for JSB, since this

nursery habitat contributes extraordinarily higher to

the recruitment of JSB compared to the vast tidal and

intertidal habitats of the Ariake Bay

Otolith microchemistry (Sr/Ca ratio) of JSB

revealed that approximately 50% of the population

that recruit to the adult stock each year from the

Ariake Bay is derived from juveniles that use nursery

areas of the Chikugo River estuary (Secor et al.1998;

Ohta 2004) Considering that the remaining 50% of

the recruits use the tidal flats as nurseries, we can

compare the nursery function of the river estuary

versus tidal flats, according to the ‘nursery role

hypothesis’ The tidal flats of Ariake Bay constitute

a total area of approximately 200 km2(Yoshikuni and

Tetsuo 2006); in contrast, the nursery area in the

Chikugo River is roughly 3.2 km2(16 km long and

0.2 km wide) Thus, the contribution per km2 of

nursery habitat to the total JSB recruitment from

Ariake Bay is 0.25% from tidal flats and as high as

15.6% from the Chikugo River estuary Clearly, river

estuary is much more important and essential as

nursery than tidal flats in Ariake Bay, based on the

‘nursery role hypothesis’ Similar contributions of

estuarine nursery grounds to fish recruitment have been

reported in other species also (Yamashita et al.2000)

According to the Beck et al (2001), only habitats

that contribute the greatest number of individuals to

the adult population on a per-unit-area basis are

considered nurseries, regardless of the overall

contri-bution that a juvenile habitat makes to the adult

population However, there are habitats that contribute

fewer individuals per-unit-area, but greater overall

number of individuals to the adult population, mainly

because of their vast area coverage; classic examples

of such habitats are tidal flats and shallow nearshore

surf zones that are used as nurseries by many species

including JSB Dahlgren et al (2006) propose theterm ‘Effective Juvenile Habitat’ (EJH) to describenursery habitats in terms of their overall contribution

to adult populations, regardless of the area coverage.Considering that the tidal flats in the Ariake Baycontributes approximately 50% to the adult population

of JSB, they should also be considered as importantnurseries for JSB according to the definition given byDahlgren et al (2006)

The importance of estuarine nursery habitats forJSB juveniles have initially been pointed out byHibino et al (1999) and Ohta (2004), but a relativelydetailed investigation was made in some of ourprevious works (Islam and Tanaka 2005, 2006a, b;Islam et al 2006a, b, c, d) where we described themechanisms that are responsible for the high values ofestuaries as nursery for juvenile JSB We found thatJSB juvenile density was higher in the estuary, wherefeeding intensity was higher, with higher growthrates, better condition and a lower starvation rate than

in the tidal flats (Table 1), suggesting that estuariesoffer a better quality habitat for juvenile JSB Similarresults highlighting and supporting the importance ofnursery habitats for JSB juveniles were supportedlater by works of Suzuki et al (2008a,b) We observedthat prey biomass was extremely high in estuarinehabitats (Hibino et al 1999; Islam et al 2006a, b,

c,d; Suzuki et al.2008a,b); we also found that meanprey size was significantly higher than those in thetidal flats Larger prey size and higher prey biomassare definite signs of a better foraging environment forJSB juveniles in the estuary Estuaries are also known

to offer specific physical environments (e.g., turbiditymaximum zone) that allow fish juveniles to co-occurwith their potential prey resources (North and Houde

2003) In addition, estuaries also offer importantpredator refuge functions since estuaries are much lessfrequented by piscivorous predators Collectively,estuaries provide JSB juveniles a completely favorableenvironment where the juveniles prosper with success-ful feeding and rapid growth that are necessary forrecruitment success

Food and feeding

JSB larvae commence exogenous feeding at day-4after hatching (Ohta 2004; Islam et al 2009a) whichcorresponds to a size of ~4.7 mm The smallest size

of JSB larvae for which diet has been reported

is ~10.0 mm SL (Nip et al 2003), and there is no

report to date on the diet of first feeding larvae Diets

of first feeding and early larvae should be restricted to

a few prey taxa because of smaller mouth gape width

(MGW) of the first feeding and early larvae MGW is

significantly and linearly related with the size of

larvae and juveniles (Nip et al.2003); the relationship

is: MGW (mm)=0.8383*SL (cm)−0.0408 (R2

=0.950)

From this relationship, the estimated MGW of first

feeding larvae is 0.36 mm Clearly, the first feeding

larvae prey on smaller zooplankton such as cyclopoid

copepods and copepod early life stages that are

reportedly highly abundant in marine environment

(Okazaki et al.2005)

Available studies on the diet of JSB larvae andjuveniles (SL ranging ~10−30 mm) at wide spatio-temporal scales and across different habitats showedthat larvae and early juveniles feed almost exclusively

on zooplankton More specifically, copepods are themost dominant component in the diet of larval JSB

in all habitats Islam et al (2006c) studied the diet

of JSB larvae and juveniles (11–30 mm SL) over

a period of 8 years covering a spatial gradient

of ~25 km in the Chikugo River estuary and foundthat copepods overwhelmingly dominated the gutcontents, contributing 83.6–100% of the diet Ahabitat-specific comparison from different studies(Table2) shows that copepods are the most dominantdiet in all habitats Copepods contributed 69.4%,

Table 2 Contribution of

copepods in the diet of

larval and juvenile Japanese

sea bass Lateolabrax

japonicus in different

habitats Feeding intensity is

the mean number of prey

total length and standard

length respectively

Table 1 Variations among the lower, middle and upper region

in an estuarine gradient (the Chikugo River estuary in Ariake

indices of larval and juvenile Japanese sea bass (JSB) Feeding

indices include size composition (%) of major prey items,

ambient water Condition indices include RNA/DNA ratio,

assigned to each value indicate significance of difference; values having different letters are significantly different (Tukey test followed by an analysis of variance)

65.0%, 85.4%, 69.3%, and 95.4% of JSB diet in

eelgrass (Zostera nana) bed, non-eelgrass bed, river

estuary, open bay, and shallow surf zone respectively

(see references in Table2) Although feeding intensity

showed remarkable variations, high copepod

contri-bution was common in all habitats

JSB is a top predator, and is highly piscivoros in

young and adult ages (Hatanaka and Sekino 1962)

Before turning to a complete piscivory, which occurs

at young stage corresponding to >60 mm SL (Nip et al

2003), JSB exhibits strong ontogenetic changes in

food habits In a long-term study, Islam et al (2006c)

showed that larvae and juveniles within 11–27 mm

SL shift diets from a mixed source composed of

several calanoid and cyclopoid copepods to a single

calanoid copepod species Gut content composition

based on prey size (Fig 2), shows that diet shift was

associated with prey size (Islam and Tanaka2006b)

The mixed diet (before shift) was dominated by small

copepods with an overall size of ~0.5 mm, which was

shifted through a median size of ~1.0 mm preys to a

final size of ~2.0 mm: thus, mean prey size also

increased consistently with fish size (Fig.2) The diet

shift was associated with transformation from larva to

juvenile stage, and once the transformation was over,

shift occurred rapidly The ontogenetic development

appeared to be associated with an increase in feeding

success, as the empty gut rates (%) reduced

exponen-tially with fish size In addition, feeding intensity also

increased significantly with fish size (Fig.2)

Nip et al (2003) reported that JSB larvae and early

Juveniles (11–20 mm SL) fed on copepods and

cladocerans, and then shifted diets to decapods and

amphipods that contributed the most part of the diet at

21–60 mm SL, and a further and complete shift to

piscivory occurred at sizes >60 mm SL (Fig 3) It

is obvious from the diet shift pattern

(copepods-cladocerans to decapods-amphipods to fish) that each

shift resulted in a substantial increase in prey biomass

Similar ontogenetic diet shift has been reported in

other studies also In the Yangtze River estuary, for

example, Sun et al (1994) reported that young sea

bass consumed mainly zooplankton, while adults fed

on small fishes and shrimps In Chikugo estuary,

Suzuki et al (2008a) reported diet shift in JSB

juveniles in a pattern in which juveniles of <40 mm

SL primarily fed on copepod preys that were

dominant in the environment, and completely

changed prey categories from copepods to mysids at

a size of 40 mm SL Shift in diet from copepods anddependence of larger juveniles on decapods andmysids was reported in other studies also (Hatanakaand Sekino1962; Hayashi and Kiyono1978).Feeding activity of larval and juvenile JSB showeddiel and tidal variations in an intertidal habitat in thesurf zone of the Ariake Bay Hibino et al (2006)reported that JSB juveniles actively fed on copepods

in the morning and the peak feeding was associatedwith high tide Similar diel patterns in feeding activitywas reported in rearing experiments and it was

0 25 50 75 100

0.0 0.5 1.0 1.5

2.0

~0.5 mm

~1.0 mm

~2.0 mm Empty gut Prey size

0 7 14 21 28 35

11 13 15 17 19 21 23 25 27

0.0 0.1 0.2

0.3

Number (FIN) Biomass (FIB)

Fish size (SL, mm)

FIN = 3.969SL 0.603 (R 2 = 0.678; p < 0.01) FIB = 0.0014SL 1.713 (R 2 = 0.937; p < 0.001)

Fig 2 Changes in prey size (mm), % empty guts, feeding

with size of larval and juvenile Japanese sea bass (JSB); larval diets that mainly composed of ~0.5 mm sized copepods were shifted to larger copepods (~2.0 mm) as the fish grew, and a complete shift was associated with transformation from larval

to juvenile stage (13–16 mm SL, indicated by the black bar) Shifting diet from smaller to larger preys was associated with a consistent decrease in % empty guts and an increase in both FIN and FIB

revealed that the peak feeding activity of JSB

juveniles (21.0 mm total length) occurred at morning

(Nanbu 1977) Hibino et al (2006) found that the

prey organisms detected in the guts at nighttime were

partially digested, which led them to suggest that

juveniles stop feeding during night, a pattern

consis-tent with the feeding behavior of the visual feeders It

was suggested that JSB juveniles migrate to the surf

zone at sunrise to feed on copepods, and then

emigrate from the surf zone at sunset, and this feeding

migration is influenced by light and tidal condition

More specifically, both the favorable light condition

and flood tide at the morning promote foraging of

JSB juveniles in the intertidal nursery habitats and the

feeding migrations are synchronized accordingly

Age, growth, mortality and recruitment potential

JSB eggs are pelagic, colorless and spherical,

mea-suring 1.35–1.44 mm in diameter with a single oil

globule but multiple oil globules were observed in

hatchery-raised eggs (Makino et al 1999) After

fertilization, hatching takes place in 4.5–5 days at

water temperature of 11.0–16.2°C and in 4.0–4.5 days

at 15.2–15.8°C (Mito 1957) Total length (TL) of

newly hatched larvae ranges 4.42–4.60 mm tion of yolk and oil globule completes in a week and

Absorp-at size ranging 5.0–5.3 mm TL TransformAbsorp-ation fromlarva to juvenile occurs at 13–17 mm SL whichcorresponds to 49–70 days of age and juvenile stagebegins at ~15 mm SL and ~60 days of age Overallgrowth rate calculated for 929 larvae and juvenilesfrom the Tango Sea ranged 0.011–0.249 mm day−1with an average of 0.132 (±0.056) mm day−1 andcorresponded closely to the previous studies (Matsu-miya et al 1985; Ohta2004)

Total length (TL, mm) − body weight (W, mg)allometry of JSB larvae and juveniles (n = 547)showed significant relationship of W=0.0032TL3.286(R2= 0.974; p < 0.001) in samples ranging 12.5–54.3 mm TL and 14.7–1464.5 mg W From ourprevious data, and modifying from our previousworks (Islam and Tanaka 2005; Islam et al.2006d),

we recomputed condition coefficient (K) of larvaland juvenile JSB in this paper as K = W*L−3*100.When computed against 10 mm size classes, mean

K increased significantly and positively (K =1.45*Ln(TL) + 7.32; R2= 0.95; p < 0.001) with fishsize (11–120 mm TL)

The instantaneous daily mortality coefficient (M)and weight-specific growth coefficient (G) are oftenused to predict cohort dynamics in fish larvae (seeHoude and Zastrow1993; Houde1997) Variations in

M, G and M/G ratio have been investigated for JSBlarvae and juveniles among years (11 years; Shoji andTanaka2007a), among cohorts within year (Shoji andTanaka 2007b), among developmental stages inAriake Bay and in Tango Sea (Islam et al unpub-lished) Values of M, G, and M/G ratio, given inTable 3 and Fig 4 show that all M, G, and M/Gexhibit high variability with cohorts, years, develop-

Fish size (SL, mm)

Fig 3 Changes in the diet of Japanese sea bass (JSB) larvae and

juveniles with size (SL, cm); JSB diet was dominated by copepods

and cladocerans in larvae and early juveniles of 1.1–2.0 cm but

was gradually replaced by decapods and amphipods as the

juveniles grow in size; juveniles turned to complete piscivory at

Table 3 Instantaneous daily mortality coefficient (M), specific growth coefficient (G) and corresponding M/G ratio of larval and juvenile Japanese sea bass in two different sites in Japan

mental stages, and locations A substantial reduction

in M/G ratio was associated with larval ontogenetic

development from preflexion to flexion stage in

Tango Sea (Table 3); in preflexion larvae, M/G ratio

was higher in Ariake Bay than in Tango Sea,

suggesting habitat-specific variations Changes in the

M/G ratio were attributed to changes in M, and not to

G We plotted M, G, and M/G values across cohorts

within a year and across 11 years (Fig.4) from Shoji

and Tanaka (2007a,b), and the plots clearly shows

that the changes in M/G ratios were closely associated

with the changes in M alone, while G was almost

constant When M was plotted against G for differentyears and different cohorts within year (Fig.5), G wasfound to significantly reduce M Available data ofM/G ratios suggest that larval and juvenile JSB lossbiomass throughout the early life (M/G >1.0) Com-parative studies (Houde and Zastrow 1993; Houde

1997) have suggested that most larval cohorts losebiomass (i.e., M > G) rapidly during early life until atransition is reached (M = G), after which biomassaccumulates (M < G) Nevertheless, there is a highdegree of variability among species in the meanweight at which the transition size (the size at which0.00

4.0 M

Fig 4 Changes in the instantaneous daily mortality coefficient

(M), weight specific growth coefficient (G) and corresponding

ratio of M/G across cohorts (upper panel) and across years

(lower panel) While G is relatively constant across cohorts and

years, M and M/G varied in a close fashion, suggesting that the

changes in M/G ratio is attributed to the changes in M, and not

in G which is usually constant, a pattern reported in many

0.02 0.05 0.08 0.11

0.00 0.03 0.06 0.09 0.12

M = −5.085G + 0.222

R2 = 0.479; p < 0.01

Weight-specific growth coefficient (G)

M = −3.766G + 0.128

R2 = 0.371; p < 0.05

Among years

Among cohorts (within year)

Fig 5 Relationship between weight specific growth coefficient (G) and instantaneous daily mortality coefficient (M) across cohorts (upper panel) and across years (lower panel) Signif- icant negative and linear relation between M and G suggest that

M decreases as G increases, both across cohorts and across

M = G) is reached, which varies with many factors

that govern the trend in either M or G, or both (Houde

1997), and is unknown for JSB

In a previous research (Islam et al.2009b,c), we

back-calculated the size-at-age and growth rate of

larvae and juveniles of JSB (n=654) in Tango Sea and

compared them among the developmental stages to

investigate if the survival of JSB larvae was

growth-and/or size-selective The study revealed that JSB

underwent strong selective survival during larval

period Individuals that survived to the juvenile stage

were larger than the larval population from which

they were sourced Larvae that had higher growth rate

and bigger size-at-age at a particular stage survived to

the next stage throughout the larval period; as such

growth rates-at-age also were higher at each stage

than the previous stage (Fig 6) However, we know

of no study reporting explicit link between early

growth rate and recruitment in JSB

Factors affecting recruitment

The early life history events described in the preceding

sections have obvious implications for recruitment,

since recruitment is determined by the processes

occurring during early life (Houde2008) Despite the

fact that recruitment problem has been one of the

central issues in fisheries research, our knowledge on

the factors that determine recruitment success and

variability in JSB is extremely limited As in most

marine fishes (Houde 2008), recruitment in JSB is

highly variable For example, Matsumiya et al (1985)

reported a 10-fold fluctuation in annual JSB

recruit-ment in the Chikugo River estuary from 1979 to

1983 They attributed the high fluctuation in

recruit-ment to density-independent survival during the larval

period since the fluctuation in the adult stock biomass

was estimated to be within only two-fold during the

same period Shoji et al (2006) reported an even

stronger, about 40-fold, fluctuation in recruitment of

JSB in the same estuary from 1990 to 2000, which

was also attributed to density-independent

mecha-nisms, governing mainly by freshwater discharge

acting through its influence on the structure and

function of estuarine nursery habitats

Shoji et al (2006) found that inter-annual variation

in recruitment of JSB did not correlate with

temper-ature, larval stage duration or river discharge

How-ever, temperature was found to significantly shortenlarval stage duration (through growth) and increase intemperature was caused by freshwater flow Theyshowed that a low freshwater discharge can reducerecruitment potential while moderate increase in thedischarge has the potential to enhance recruitmentthrough increasing larval growth rate via increases intemperature and perhaps also via enhanced preyproduction A further increase in freshwater flow,however, affected recruitment negatively as theyfound that in high-flow years, recruitment was poor

0.000.060.120.180.240.30

0481216

PreflexionFlexionPostflexionJuvenile

at each daily age of Japanese sea bass, showing growth- and selective survival Most values are significantly different among four stages (repeated measures analysis of variance)

despite high temperature and apparent good growth It

was speculated that a high freshwater discharge may

have a‘wash-out’ effect, carrying prey resources out

of the estuary and preventing the larvae and juveniles

to immigrate into nursery habitats Shoji and Tanaka

concluded that JSB recruitment is successful in years

with intermediate temperature, short larval stage

duration and moderate river discharge Thus,

variabil-ity in freshwater discharge is an important

determi-nant of recruitment in estuarine-dependent fishes,

such as JSB

In another study, Shoji and Tanaka (2007b) found

that recruitment variations among cohorts of JSB

within a year was strongly influenced by temperature

that enhance prey production, promote larval and

juvenile growth, reduce mortality and increase

recruit-ment potential As such, cohorts that appear later in a

year experience favourable temperature and prey field

than their counterparts appearing earlier and therefore

have greater potential for recruitment Rearing

experi-ments reported that swimming performance and gastric

evacuation rate of JSB larvae and juveniles increased

with the increase in temperature within a range of 13–

23°C (Hirata1967) Within range, temperature

gener-ally has positive effects on early growth and survival

of estuarine fishes (Secor and Houde1995; Limburg

et al 1999; Sirois and Dodson 2000) At low

temperatures, larval ability to avoid predators

decreases due to decreased swimming performance

(Hunter 1981) In addition, larval duration becomes

prolonged due to decreased ingestion and growth,

increasing the probability of accumulated mortality

(Houde 1987) Larvae with low ingestion rate and

poor condition may lose behavioural integrity

neces-sary to survive in fluctuating environment in estuaries

(Sirois and Dodson2000; North and Houde2003)

In a previous study, we investigated (Islam et al in

review) the recruitment in four different cohorts of

JSB in Tango Sea at the Japan Sea coast and found

that the density of recruits had no significant

relationship with the temperature experienced by the

members of the cohorts from hatching to settlement

Also, variation in recruitment among cohort was not

related to the average growth rates experienced by the

members of the cohorts Multiple regression analysis

revealed that recruitment variation was significantly

affected by the initial density of larvae (i.e., larval

supply) which explained >97% of the variability in

recruitment among cohorts In this way, we speculate

that inter-annual variation in larval supply can alsodrive year-to-year variability in recruitment However,within each cohort, recruitment was strongly depen-dent on growth rate, in such that individuals that grewfaster during larval period selectively survived tobecome juveniles (recruits), a pattern consistent withnumerous studies reporting growth-dependent recruit-ment in a variety of fishes (see Takasuka et al 2004and the references therein) We found that thisselection for fast growth within cohort occurredindependent of temperature, simply because members

of a cohort should experience the same physicalcondition in the field We also found evidence that atleast in part, individual fitness for survival wascontributed from parental sources, in such that somelarvae were bigger at hatch and grew faster before theonset of exogenous feeding, suggesting parentalinfluence on the survival process and therefore onsubsequent recruitment

In summary, recruitment in estuarine dependentfishes such as JSB is determined by interplay amongmyriad of factors that are spatio-temporally specific.This also explains why studies have reported con-trasting scenarios on the factors affecting JSBrecruitment In addition, the definition of ‘recruit-ment’ and of ‘cohort’ differed widely in differentstudies and seems to have greatly affected conclusionsmade in each study Overall, temperature, preyconcentration and larval supply have positive influ-ence on JSB recruitment while both high and lowfreshwater discharges can have negative effects

Impacts of climate change

In recent years, a great deal of attention has been paid

to the effects of climate change on coastal and marineecosystems, and substantial discussions have beenmade on the impacts of climate change on differentlevels of ecological organization, from plankton(Richardson and Schoeman 2004; Hays et al 2005)

to fish (Drinkwater2005; Perry et al.2005; Rijnsdorp

et al 2009) However, the early life history of fisheshas not received much attention from a climatechange context For many reasons, early life stagesare more vulnerable to climate-induced changes thantheir adult counterparts (Rijnsdorp et al.2009) This isparticularly true for fishes that exhibit a migratory lifehistory during their early life and thus require

connectivity among habitats (Rijnsdorp et al.2009) as

in the case of JSB In this section, we look at the

possibility that climate-induced changes have already

affected JSB early life history and recruitment and

discuss the possible effects that may occur in future

Historical (1901–2009) temperature (air

tempera-ture, used as proxy for sea surface temperature) and

precipitation (used as proxy for freshwater discharge)

data were collected from Japan Meteorological Agency

(www.jma.go.jp) and are plotted as mean values

combined for winter and spring (January-April; period

of JSB larval and early juvenile development) each

year as well as annual mean Temperature has

increased remarkably around Japanese coastal waters

over the past decades; starting since 1950s,

tempera-ture still continues to rise (Fig 7) In recent decades,

temperature increase has been much more rapid than

ever While a rise in 0.85°C occurred over the last

60 years, during the last 21 years average temperature

increased by 1.25°C In contrast, mean precipitation

showed no change over the century although there

were obvious inter-annual fluctuations (Fig 7) Mean

precipitation during 1960–2009 (106 mm in

winter-spring and 142 mm annual) was almost the same as the

mean during 1901–1960 (105 mm in winter−spring

and 143 mm annual)

It is difficult to ascertain if a 1.25°C rise in

temperature over the last 21 years have had any effect

on JSB early life history and recruitment However,

available literature on temperature effects on early life

history and recruitment of JSB discussed in the

preceding section led us to believe that climate

change have had a positive impact on JSB, or at least

have not impacted negatively Commercial catch of

JSB has been increasing since the early 1950s,

suggesting successful recruitment of JSB, and

indi-cating further that the rise in temperature has not

affected the early life history of JSB and recruitment

Indeed, we found no correlation between JSB catch

and temperature over a period of 55 years, from 1950

to 2004 (Fig 8) No change in precipitation

(there-fore, freshwater discharge) during 1901–2009 implies

that in Japanese coastal waters, the rate of freshwater

discharge has not been changed as predicted (IPCC

2007), and therefore has not adversely affected JSB

recruitment However, inter-annual variations in JSB

catch was negatively and significantly affected by

mean inter-annual winter-spring precipitation (Fig.8)

although mean annual precipitation did not have

significant influence on JSB catch Since spring precipitation corresponds to the period of larvaland juvenile development, it might have affected JSBcatch through its influence on recruitment Thisimplies that any significant change in precipitationpattern due to future climate change may negativelyaffect JSB fishery

winter-It has been suggested that JSB will exhibit a shift

in geographical distribution toward the pole inresponse to future climate change Projected change

in JSB distribution by year 2050 (see Froese andPauly 2009 and www.fishbase.org) shows that JSBwill shift to the north along the Chinese (the YellowSea), Korean (the West Sea) as well as the Japanesecoasts According to the prediction, JSB will moveapproximately 200 km in the Yellow Sea and the WestSea and even further northward, by approximately

300 km in Japanese coastal waters By implication,this poleward shift in distribution can have a range ofpossible consequences that are mostly unpredictable.Proposed hypotheses (Rijnsdorp et al 2009) on theeffects of climate change suggest that populations thatare more vulnerable to climate change are those that(1) are at the limits of their latitudinal range ratherthan occurring in the centre of their latitudinal range;(2) are with narrow dietary preferences rather thanbeing generalists; (3) require spatially restrictedhabitat during part of their life history requirements;and (4) under intense exploitation Comparing theearly life history of JSB with these proposedhypotheses, we speculate that JSB is less likely to

be affected by small-to-moderate level of climatechange in future because (1) JSB is well within itslatitudinal range and has been reported to performwell within a wide range of temperature; (2) JSB,particularly juvenile and adults feed on a wide variety

of prey resources and can actively select and shiftdiets; (3) although estuarine and nearshore habitatsare necessary for larvae and juveniles, they are notrestricted to spatially narrow range of habitats;moreover, a high degree of physiological (e.g.,adaptation to low salinity; Hirai et al 1999) andbehavioural (synchronization of diel movements forfeeding and transport; see above) adaptability allowJSB to prosper in a wide variety of habitat types; and(4) the JSB stock has been exploited sustainably as isevident form increased commercial catch since 1950s.Nevertheless, JSB early life stages can be affected byfuture climate change in an indirect manner through a

number of alternative mechanisms such as by altering

the physical environment and/or affecting at different

levels of the trophic pathways on which the fish

depends A detailed discussion on the mechanisms

how climate change can act on ecosystems and on

organisms can be found elsewhere (Drinkwater et al

2010) Obviously, the degree to which JSB will be

affected by future climate change will depend on

many factors including the degree of future climate

change as well as the human pressure on the current

stock of the fish and on the ecosystem

Future research

Although substantial amount of works have beendone during the last few years, many aspects ofthe early life history and ecology of JSB remainunknown In addition, existing studies cover onlynarrow spatial scales, although JSB is distributedwidely in the coastal waters around Japan Thus, amajor gap exists in the spatio-temporal resolution inthe early life ecology and the corresponding recruit-ment variability Early life of estuarine dependent

04080120160200

Winter-Spring Annual

121314151617

5678910

panel) and temperature

(lower panel) data

collected at 30 stations

covering the areas of

Japanese sea bass (JSB)

distribution Annual

data are average values

of 12 months (all 30

stations) and winter-spring

data are average of

all 30 stations) that

correspond to the period

of larval and juvenile

JSB occurrence

fishes can be particularly challenging because their

spawning grounds are located distant from nursery

areas Larvae require appropriate currents and

suffi-cient and suitable food during transit to reach the

nursery area at the proper time, size, and condition

Meteorologic and oceanographic factors that

influ-ence food availability and transport direction and time

and variations in these factors at any dimension could

greatly affect recruitment success The details of the

coupling of spawning to natural oceanographic

transport systems for eggs and larvae, and the

consequences of deviations from usual transport

mechanisms remain unstudied Future research should

look to resolve these details, including environmental

cues to reproductive behavior and relative importance

of passive and behaviorally mediated transport

JSB juveniles have been reported to utilize

different types of nearshore and estuarine habitats as

nurseries; the relative importance of each of these

habitats in growth survival and recruitment of JSB has

not been quantified Identification of the “effective

juvenile habitats (EJH)” for juvenile growth and

survival is important, since information on EJH cangreatly facilitate management and conservation deci-sion (Dahlgren et al 2006) Establishing linksbetween habitat utilization by larvae and juvenilesand corresponding contribution to recruitment isessential In addition, larger habitats may be com-prised of a number of relatively smaller habitats ofvarying kinds For example a tidal flat may becomprised of any combination of vegetated, non-vegetated, sandy, muddy, oyster bed etc and theymay serve differentially for juvenile recruitment.Therefore, nursery functions of larger habitats should

be scrutinized at finer scales

In order to better understand recruitment nisms, identification of the periods that are critical forlarval survival is important The prevailing concept isthat in most marine fishes, the critical periodcorresponds to the first feeding, and recruitmentvariability is regulated largely by the level of preyabundance at that time (see review by Houde 2008)

mecha-In JSB, however, we have found that a potentialcritical period may correspond to the metamorphosis

0 3 6 9 12

0 3 6 9

launAl

aunA

Winter & Spring Winter & Spring

Japanese sea bass (JSB)

around Japanese coastal

(Islam and Tanaka2006b), and the critical period was

associated with the availability of suitable prey during

a diet shift No information is available on the first

feeding of JSB larvae and the associated crises in the

field, and should be included in future research

Future studies should also examine if any critical

period corresponds to elevated mortality

Understand-ing on habitat- and stage-specific changes in growth

and mortality coupled with spatio-temporal variations

in oceanographic features are essential in predicting

recruitment variability

In recent decades, climate-induced changes have

put forward new questions, hypotheses and challenges

to marine ecologists, fisheries scientists and managers

There is now ample evidence that climate changes have

already affected coastal and marine ecosystems

includ-ing fish and fisheries in different parts of the world

(IPCC 2007) Since early life stages are more

vulnerable to environmental change and since

recruit-ment and stock size depend largely on the early life

demography, an effective management strategy should

focus on early life processes In doing so, we need

detailed understanding on the ecosystem processes that

act on the early life of JSB; we also need to understand

the sensitivity of these processes to potential future

environmental changes Such processes should be

studied and compared across habitats and ecosystems

to formulate effective management tools such as an

ecosystem model or recruitment model

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Genetic structure of the white croaker, Micropogonias

furnieri Desmarest 1823 (Perciformes: Sciaenidae)

along Uruguayan coasts: contrasting marine,

estuarine, and lacustrine populations

Alejandro D’Anatro&Alfredo N Pereira&

Enrique P Lessa

Received: 9 July 2010 / Accepted: 23 March 2011 / Published online: 8 April 2011

# Springer Science+Business Media B.V 2011

Abstract Micropogonias furnieri is widely distributed

in the southwestern Atlantic Ocean In Uruguay,

Laguna de Rocha and Río de La Plata estuary have

been reported as reproductive and nursery areas In

Laguna de Rocha, individuals reach maturity at

smaller total length than their oceanic counterparts

It has been difficult to establish whether Laguna de

Rocha represents a biologically distinct population or

simply ecophenotypic variation More generally, the

possible presence of several distinct populations of

white croakers in Uruguayan waters has been

hypoth-esized, but limited data exist to substantiate them A

recent mitochondrial DNA analysis suggested

diver-gence between the Río de La Plata and the Oceanic

front populations Using seven microsatellites loci, we

studied the population structure of M furnieri in the

nursery areas suggested by the literature, as well as in

three additional localities to test these hypotheses

The individuals of Laguna de Rocha showed a

moderate genetic differentiation with respect to some

of the other populations surveyed Specimens ofMontevideo showed the higher genetic distinctive-ness Given the apparent absence of geographicalbarriers, other factors may be responsible for theobserved differentiation The complex pattern offorces interacting in this system makes it difficult todisentangle the causes of the population structurefound The adaptation to local environmental con-ditions could be playing an important role inpopulation differentiation, as well as the possibleselective pressures imposed by fisheries The resultsobtained in this work offer clues about the processesresponsible for differentiation of fishes in estuarineand marine environments

Keywords Estuarine differentiation Microsatellites Population genetics Size reduction in fishes

Introduction

Coastal marine environments have been considered ashighly dynamic areas from the standpoint of historicalbiogeography (Beheregaray et al 2002) Amongthem, estuaries constitute interesting systems to testthe role of ecological factors in promoting populationdifferentiation in marine fishes, because of theecological distinctiveness of these environments com-pared to strictly oceanic areas The white croaker,Micropogonias furnieri, represents a good model to

DOI 10.1007/s10641-011-9799-x

Departamento de Ecología y Evolución,

Facultad de Ciencias, Universidad de la República,

Iguá 4225,

CP11400 Montevideo, Uruguay

e-mail: passer@fcien.edu.uy

A N Pereira

Dirección Nacional de Recursos Acuáticos (DINARA),

Ministerio de Ganadería Agricultura y Pesca (MGAP),

Constituyente 1497,

CP11200, P.O BOX 1612, Montevideo, Uruguay

examine ecological differentiation between these

systems (i.e ocean and estuary), since this species is

commonly found inhabiting estuaries along its wide

distribution White croakers are distributed along the

Atlantic coast, from Mexico (20°N) to the Gulf of San

Matías, Argentina (41°S) (Isaac1988; Vazzoler 1991)

This species is one of the most important economic

fishery resources in Uruguay (DINARA 2003), and it

is also exploited in countries such as Venezuela,

Guyanas, Brazil and Argentina (Haimovici et al

1989; Vazzoler1991; Alvárez and Pomares1997)

Like other Sciaenidae, white croakers move

inshore during the reproductive season In Uruguay,

M furnieri reproduces during spring and summer

(Acuña et al 1992), and in some cases individuals

enter into rivers and coastal lagoons These

environ-ments act as nursery areas, including Laguna de

Rocha and the Río de La Plata estuary in Uruguay

(Vizziano et al 2002 and references therein) In

Laguna de Rocha, individuals that reach maturity

are 11–12 cm smaller than those from the Atlantic

Ocean, which attain maturity at approximately 30 cm

of total length (Vizziano et al 2002) A similar

phenomenon had been reported for the same species

on other coastal lagoon, Lagoa dos Patos, in southern

Brazil (Castello1986; Haimovici and Gatto1996) and

also for other species which inhabits estuaries (e.g

Micropogonias undulatus Linnaeus 1766; Ross

1988) Further yet, it has been proposed that this

strategy, i.e small asymptotic size and sexual

matu-rity at an earlier stage, is adopted by organisms that

suffer elevated mortality rates (Ross1988) This size

reduction in sexually mature organisms may be a

response to strong selection against the largest

individuals in certain environments Several

mecha-nisms have been proposed to explain character

displacement in these cases (see Ratner and Lande

2001) with special emphasis in the selective pressures

imposed by fisheries Commercial fisheries, in

partic-ular, target large fish; in this way individuals

genetically predisposed to mature at later stages of

life or at larger sizes are selected against Thus,

fisheries may act as a selective force favoring

individuals genetically predisposed to mature at

earlier stages of life and/or at smaller sizes (Browman

2000; Ernande et al 2003; Stockwell et al 2003;

Hutchings 2004; Olsen et al 2004; Stenseth and

Rouyer2008) A small artisanal fishing fleet operates

in the Laguna de Rocha (Santana and Fabiano1999),

and M furnieri is mainly captured as by-catch offisheries focused on other species (fishes: e.g.Brevoortia aurea, Odonthestes argentinensis andshrimps: e.g Penaeus paulensis) (Saona et al.2003).Fishing appears to have low impact over whitecroaker population of Laguna de Rocha, but it hasnot been properly analyzed yet It is also possible thatnatural, non-human selective factors favor maturation

at younger ages and/or smaller sizes Additionally,such size reduction may be simply due to phenotypicplasticity (see discussion)

Analyzing size structure, Cotrina (1986) proposedthe existence of two populations of M furnieri: one inthe Río de La Plata estuary to latitude 38°S, and theother in El Rincón (40°S, Argentina) It was alsoreported by Cotrina (1986) that at higher latitudes thefemales were in gonadal repose, whereas at the sametime (autumn), the percentage of females that recentlyspawn was higher in southern regions However, itwas also suggested that these differences may besimply the response to a more intense use of thisresource in the Río the La Plata area A similardifferentiation pattern was mentioned in Figueroa andDíaz de Astarloa (1991) Galli (2001), on the basis ofmorphometric and meristic characters, found evidence

of differentiation between white croakers from Río de

La Plata estuary and Uruguayan Atlantic waters

In contrast with these morphological studies,Maggioni et al (1994) found extensive gene flowbetween Rio Grande (33°S, Brazil) and El Rincón in

an allozyme survey, and concluded that these regionshost a single panmictic population of white croakers.Similar studies suggested high levels of gene flowbetween the Río de La Plata and its oceanic front(Pereira 1990) More recently, Pereira et al (2009)using mitochondrial DNA (mtDNA) as a molecularmarker, found moderate levels of gene flow betweenindividuals from Río de La Plata and its oceanicfront Like in Uruguayan waters, a study using RFLPs

of mtDNA (Puchnik-Legat and Levy 2006) foundrestricted gene flow among several populations alongthe Brazilian coast (see discussion) Likewise, differ-ent stocks had been proposed for Brazilian waters bymeans of morphological analyses (e.g Vazzoler1971;Haimovici and Gatto 1996), but all these findingswere not evidenced in previous allozyme studies(Levy et al.1998)

In sum, morphological and meristic analysesindicated the existence of a population at Río de La